Cilia-based peptidergic signaling

Peptide-based intercellular communication is a ubiquitous and ancient process that predates evolution of the nervous system. Cilia are essential signaling centers that both receive information from the environment and secrete bioactive extracellular vesicles (ectosomes). However, the nature of these...

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Bibliographic Details
Published in:PLoS biology 2019-12, Vol.17 (12), p.e3000566-e3000566
Main Authors: Luxmi, Raj, Kumar, Dhivya, Mains, Richard E, King, Stephen M, Eipper, Betty A
Format: Article
Language:English
Subjects:
Aquatic plants
Biology and Life Sciences
Biophysics
Cell Communication - physiology
Cell signaling
Cell-Derived Microparticles - metabolism
Chlamydomonas
Chlamydomonas - metabolism
Chlorophyta - metabolism
Cilia
Cilia - metabolism
Cilia - physiology
Endoplasmic reticulum
Enzymes
Eukaryotes
Gametes
Genomes
Insects
Mixed Function Oxygenases - metabolism
Molecular biology
Monooxygenase
Multienzyme Complexes - metabolism
Nervous system
Neuropeptides
Neurosciences
Peptides
Peptides - metabolism
Proteins
Receptors
Research and Analysis Methods
Signal Transduction - physiology
Signaling
Subtilisin
Supervision
Tumor necrosis factor-TNF
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Summary:Peptide-based intercellular communication is a ubiquitous and ancient process that predates evolution of the nervous system. Cilia are essential signaling centers that both receive information from the environment and secrete bioactive extracellular vesicles (ectosomes). However, the nature of these secreted signals and their biological functions remain poorly understood. Here, we report the developmentally regulated release of the peptide amidating enzyme, peptidylglycine α-amidating monooxygenase (PAM), and the presence of peptidergic signaling machinery (including propeptide precursors, subtilisin-like prohormone convertases, amidated products, and receptors) in ciliary ectosomes from the green alga Chlamydomonas. One identified amidated PAM product serves as a chemoattractant for mating-type minus gametes but repels plus gametes. Thus, cilia provide a previously unappreciated route for the secretion of amidated signaling peptides. Our study in Chlamydomonas and the presence of PAM in mammalian cilia suggest that ciliary ectosome-mediated peptidergic signaling dates to the early eukaryotes and plays key roles in metazoan physiology.
ISSN:1545-7885
1544-9173
1545-7885
DOI:10.1371/journal.pbio.3000566